Genomic and Multi-Omics Analysis of Phlebopus portentosus: Effects of Cultivation on Secondary Metabolites

<i>Phlebopus portentosus</i> is an edible and medicinal ectomycorrhizal mushroom with delicious and high nutritional value. However, the mechanism of secondary metabolite biosynthesis in <i>P. portentosus</i> is still unclear. In this study, the genomics, metabolomics, and transcriptomics were integrated to reveal the biosynthesis mechanism of secondary metabolites in <i>P. portentosus</i> under different cultivation conditions. The 31.4 Mb genome of <i>P. portentosus</i> YAF023 with 15 scaffolds was assembled by Illumina and Nanopore sequencing and annotated, and 206 cytochrome P450s, 201 carbohydrate-active enzymes, 186 transcription factors, 18 terpene synthases (TPSs), and 5 polyketide synthases (PKSs) were identified. Multi-omics analysis showed that <i>PpPKS1</i> is probably involved in the biosynthesis of Ethyl orsellinate; <i>PpPKS2</i> and <i>PpPKS5</i> are probably involved in the synthesis of 6-Methylsalicylic acid and Cytochalasin Z5, respectively; <i>PpTRI5</i> was involved in the tetracyclic sesquiterpene <i>β</i>-type trichodiene compounds; and <i>PpSTCs</i> was involved in the synthesis of β-copaene analogs or derivatives. Co-expression network analysis and binding site prediction of the promoter regions suggested that <i>PpHOX4</i> and <i>PpHSF1</i> regulated the gene expression of <i>PpPKS1</i>, and <i>Ppzf-C2H2 32</i> and <i>PpHSF5</i> regulated the gene expression of <i>PpSTCs 8</i>, and <i>PpSTCs 3,</i> respectively. This study will provide an important foundation for further development and utilization of secondary metabolites of <i>P. portentosus</i>.